Electrophysiology of synaptic vesicle cycling.

Patch-clamp capacitance measurements can monitor in real time the kinetics of exocytosis and endocytosis in living cells. We review the application of this technique to the giant presynaptic terminals of goldfish bipolar cells. These terminals secrete glutamate via the fusion of small, clear-core vesicles at specialized, active zones of release called synaptic ribbons. We compare the functional characteristics of transmitter release at ribbon-type and conventional synapses, both of which have a unique capacity for fast and focal vesicle fusion. Subsequent rapid retrieval and recycling of fused synaptic vesicle membrane allow presynaptic terminals to function independently of the cell soma and, thus, as autonomous computational units. Together with the mobilization of reserve vesicle pools, local cycling of synaptic vesicles may delay the onset of vesicle pool depletion and sustain neuronal output during high stimulation frequencies.

[1]  M. Tachibana,et al.  Submillisecond Kinetics of Glutamate Release from a Sensory Synapse , 1998, Neuron.

[2]  Venkatesh N. Murthy,et al.  Synaptic vesicles retain their identity through the endocytic cycle , 1998, Nature.

[3]  R. Heidelberger Adenosine Triphosphate and the Late Steps in Calcium-dependent Exocytosis at a Ribbon Synapse , 1998, The Journal of general physiology.

[4]  Oleg Shupliakov,et al.  Sustained Neurotransmitter Release: New Molecular Clues , 1997, The European journal of neuroscience.

[5]  E. Neher,et al.  Multiple Forms of Endocytosis In Bovine Adrenal Chromaffin Cells , 1997, The Journal of cell biology.

[6]  G. Alvarez de Toledo,et al.  The exocytotic event in chromaffin cells revealed by patch amperometry , 1997, Nature.

[7]  A. Vyshedskiy,et al.  Change of transmitter release kinetics during facilitation revealed by prolonged test pulses at the inhibitor of the crayfish opener muscle. , 1997, Journal of neurophysiology.

[8]  T. Schikorski,et al.  Quantitative Ultrastructural Analysis of Hippocampal Excitatory Synapses Materials and Methods Terminology Fixation and Embedding , 2022 .

[9]  G. Matthews,et al.  Static and dynamic membrane properties of large-terminal bipolar cells from goldfish retina: experimental test of a compartment model. , 1997, Journal of neurophysiology.

[10]  E Neher,et al.  Estimation of mean exocytic vesicle capacitance in mouse adrenal chromaffin cells. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[11]  C. Stevens,et al.  Heterogeneity of Release Probability, Facilitation, and Depletion at Central Synapses , 1997, Neuron.

[12]  E. Brown,et al.  Assessment of frequency-dependent alterations in the level of extracellular Ca2+ in the synaptic cleft. , 1997, Biophysical journal.

[13]  M. Tachibana,et al.  Two components of transmitter release in retinal bipolar cells: exocytosis and mobilization of synaptic vesicles , 1997, Neuroscience Research.

[14]  G. Matthews,et al.  Depletion and Replenishment of Vesicle Pools at a Ribbon-Type Synaptic Terminal , 1997, The Journal of Neuroscience.

[15]  R. Zucker,et al.  Exocytosis: A Molecular and Physiological Perspective , 1996, Neuron.

[16]  G. Matthews,et al.  Ultrafast Exocytosis Elicited by Calcium Current in Synaptic Terminals of Retinal Bipolar Neurons , 1996, Neuron.

[17]  H. Wässle,et al.  A SNARE Complex Containing Syntaxin 3 Is Present in Ribbon Synapses of the Retina , 1996, The Journal of Neuroscience.

[18]  Leon Lagnado,et al.  Continuous Vesicle Cycling in the Synaptic Terminal of Retinal Bipolar Cells , 1996, Neuron.

[19]  K. Ikeda,et al.  Synaptic vesicles have two distinct recycling pathways , 1996, The Journal of cell biology.

[20]  B. Sakmann,et al.  Calcium influx and transmitter release in a fast CNS synapse , 1996, Nature.

[21]  W. Betz,et al.  Nerve Activity but Not Intracellular Calcium Determines the Time Course of Endocytosis at the Frog Neuromuscular Junction , 1996, Neuron.

[22]  M. Dichter,et al.  Calcium-dependent Paired-pulse Facilitation of Miniature Epsc Frequency Accompanies Depression of Epscs at Hippocampal Synapses in Culture , 1996 .

[23]  A. Oberhauser,et al.  Simultaneous capacitance and amperometric measurements of exocytosis: a comparison. , 1996, Biophysical journal.

[24]  M. Jackson,et al.  Rapid exocytosis and endocytosis in nerve terminals of the rat posterior pituitary. , 1996, The Journal of physiology.

[25]  Y. Miyashita,et al.  Two components of exocytosis and endocytosis in phaeochromocytoma cells studied using caged Ca2+ compounds. , 1996, The Journal of physiology.

[26]  P. Smith,et al.  Endocytosis of secretory granules in mouse pancreatic beta‐cells evoked by transient elevation of cytosolic calcium. , 1996, The Journal of physiology.

[27]  W. Almers,et al.  Fast steps in exocytosis and endocytosis studied by capacitance measurements in endocrine cells , 1996, Current Opinion in Neurobiology.

[28]  G. Matthews,et al.  Evidence That Vesicles on the Synaptic Ribbon of Retinal Bipolar Neurons Can Be Rapidly Released , 1996, Neuron.

[29]  S. J. Smith,et al.  The timing of synaptic vesicle endocytosis. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[30]  E. A. Schwartz,et al.  Asynchronous transmitter release: control of exocytosis and endocytosis at the salamander rod synapse. , 1996, The Journal of physiology.

[31]  W. Betz,et al.  Simultaneous independent measurement of endocytosis and exocytosis , 1996, Nature.

[32]  P. Camilli,et al.  Molecular Mechanisms in Synaptic Vesicle Endocytosis and Recycling , 1996, Neuron.

[33]  S. Laughlin,et al.  The rate of information transfer at graded-potential synapses , 1996, Nature.

[34]  G. Matthews,et al.  Calcium-dependent inactivation of calcium current in synaptic terminals of retinal bipolar neurons , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[35]  A. Henkel,et al.  Staurosporine blocks evoked release of FM1-43 but not acetylcholine from frog motor nerve terminals , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[36]  H. Reuter,et al.  Localization and functional significance of the Na+/Ca2+exchanger in presynaptic boutons of hippocampal cells in culture , 1995, Neuron.

[37]  H. Horstmann,et al.  Docked granules, the exocytic burst, and the need for ATP hydrolysis in endocrine cells , 1995, Neuron.

[38]  C. Zorumski,et al.  Paired‐pulse modulation of fast excitatory synaptic currents in microcultures of rat hippocampal neurons. , 1995, The Journal of physiology.

[39]  M. McNiven,et al.  Rapid endocytosis coupled to exocytosis in adrenal chromaffin cells involves Ca2+, GTP, and dynamin but not clathrin. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[40]  M. Turelli,et al.  The kinetics of quantal transmitter release from retinal amacrine cells. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[41]  Thomas C. Südhof,et al.  The synaptic vesicle cycle: a cascade of protein–protein interactions , 1995, Nature.

[42]  Paul Greengard,et al.  Distinct pools of synaptic vesicles in neurotransmitter release , 1995, Nature.

[43]  R. Tsien,et al.  Properties of synaptic transmission at single hippocampal synaptic boutons , 1995, Nature.

[44]  H. Atwood,et al.  Synaptic differentiation of a single motor neuron: conjoint definition of transmitter release, presynaptic calcium signals, and ultrastructure , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[45]  W G Regehr,et al.  Calcium transients in cerebellar granule cell presynaptic terminals. , 1995, Biophysical journal.

[46]  Stephen J. Smith,et al.  Vesicle pool mobilization during action potential firing at hippocampal synapses , 1995, Neuron.

[47]  Heinrich Betz,et al.  From vesicle docking to endocytosis: Intermediate reactions of exocytosis , 1995, Neuron.

[48]  M. Lindau,et al.  The exocytotic fusion pore of small granules has a conductance similar to an ion channel , 1995, The Journal of cell biology.

[49]  S. Schmid,et al.  Tubular membrane invaginations coated by dynamin rings are induced by GTP-γS in nerve terminals , 1995, Nature.

[50]  Zhuan Zhou,et al.  Action Potential-induced Quantal Secretion of Catecholamines from Rat Adrenal Chromaffin Cells (*) , 1995, The Journal of Biological Chemistry.

[51]  M. Tachibana,et al.  Ca2+ regulation in the presynaptic terminals of goldfish retinal bipolar cells. , 1995, The Journal of physiology.

[52]  C. Stevens,et al.  Estimates for the pool size of releasable quanta at a single central synapse and for the time required to refill the pool. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[53]  K. Gillis Techniques for Membrane Capacitance Measurements , 1995 .

[54]  E Neher,et al.  Time course of Ca2+ concentration triggering exocytosis in neuroendocrine cells. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[55]  Y. Goda,et al.  Two components of transmitter release at a central synapse. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[56]  T. Südhof,et al.  Synaptotagmin I: A major Ca2+ sensor for transmitter release at a central synapse , 1994, Cell.

[57]  S. Borges,et al.  Control of transmitter release from retinal amacrine cells by Ca2+ influx and efflux , 1994, Neuron.

[58]  Richard J. Bookman,et al.  Releasable pools and the kinetics of exocytosis in adrenal chromaffin cells , 1994, Neuron.

[59]  Gary Matthews,et al.  Calcium dependence of the rate of exocytosis in a synaptic terminal , 1994, Nature.

[60]  W. Almers,et al.  Calcium-triggered exocytosis and endocytosis in an isolated presynaptic cell: Capacitance measurements in saccular hair cells , 1994, Neuron.

[61]  F. Werblin,et al.  Miniature excitatory postsynaptic currents in bipolar cells of the tiger salamander retina , 1994, Vision Research.

[62]  Gary Matthews,et al.  Inhibition of endocytosis by elevated internal calcium in a synaptic terminal , 1994, Nature.

[63]  W. Almers,et al.  A triggered mechanism retrieves membrane in seconds after Ca(2+)- stimulated exocytosis in single pituitary cells , 1994, The Journal of cell biology.

[64]  H. V. Gersdorff,et al.  Dynamics of synaptic vesicle fusion and membrane retrieval in synaptic terminals , 1994, Nature.

[65]  J. Meldolesi,et al.  Neurotransmitter release: fusion or 'kiss-and-run'? , 1994, Trends in cell biology.

[66]  E. Neher,et al.  A Ca-dependent early step in the release of catecholamines from adrenal chromaffin cells. , 1993, Science.

[67]  Stephen J. Smith,et al.  The kinetics of synaptic vesicle recycling measured at single presynaptic boutons , 1993, Neuron.

[68]  Richard Robitaille,et al.  Functional colocalization of calcium and calcium-gated potassium channels in control of transmitter release , 1993, Neuron.

[69]  T. Südhof,et al.  Dynamin GTPase regulated by protein kinase C phosphorylation in nerve terminals , 1993, Nature.

[70]  J. R. Monck,et al.  GTPγS stimulates exocytosis in patch-clamped rat melanotrophs , 1993, Neuron.

[71]  M. Tachibana,et al.  Dihydropyridine-sensitive calcium current mediates neurotransmitter release from bipolar cells of the goldfish retina , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[72]  P. Katz,et al.  Facilitation and depression at different branches of the same motor axon: evidence for presynaptic differences in release , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[73]  J. M. Fernández,et al.  Release of secretory products during transient vesicle fusion , 1993, Nature.

[74]  S. Borges,et al.  Synaptic transmission between pairs of retinal amacrine cells in culture , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[75]  Hans-Joachim Wagner,et al.  Spinules: a case for retinal synaptic plasticity , 1993, Trends in Neurosciences.

[76]  S. Yazulla,et al.  Goldfish bipolar cells and axon terminal patterns: A Golgi study , 1993, The Journal of comparative neurology.

[77]  F Benfenati,et al.  Synaptic vesicle phosphoproteins and regulation of synaptic function. , 1993, Science.

[78]  W. Betz,et al.  Optical monitoring of transmitter release and synaptic vesicle recycling at the frog neuromuscular junction. , 1993, The Journal of physiology.

[79]  H. Plattner,et al.  Exo-endocytosis in isolated peptidergic nerve terminals occurs in the sub-second range , 1992, Bioscience reports.

[80]  H Korn,et al.  Intrinsic quantal variability due to stochastic properties of receptor-transmitter interactions. , 1992, Science.

[81]  P. Maycox,et al.  Clathrin-coated vesicles in nervous tissue are involved primarily in synaptic vesicle recycling , 1992, The Journal of cell biology.

[82]  J. Nordmann,et al.  Membrane retrieval following exocytosis in isolated neurosecretory nerve endings , 1992, Neuroscience.

[83]  S. Yazulla,et al.  Light‐dependent plasticity of the synaptic terminals of Mb bipolar cells in goldfish retina , 1992, The Journal of comparative neurology.

[84]  P. De Camilli,et al.  Exo-endocytotic recycling of synaptic vesicles in developing processes of cultured hippocampal neurons , 1992, The Journal of cell biology.

[85]  E Neher,et al.  Calcium requirements for secretion in bovine chromaffin cells. , 1992, The Journal of physiology.

[86]  G. Matthews,et al.  Calcium influx and calcium current in single synaptic terminals of goldfish retinal bipolar neurons. , 1992, The Journal of physiology.

[87]  K. Zipser,et al.  Role of residual calcium in synaptic depression and posttetanic potentiation: Fast and slow calcium signaling in nerve terminals , 1991, Neuron.

[88]  W. Almers,et al.  Millisecond Studies of Single Membrane Fusion Events a , 1991, Annals of the New York Academy of Sciences.

[89]  T Okada,et al.  Release of endogenous excitatory amino acids from ON-type bipolar cells isolated from the goldfish retina , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[90]  M. Charlton,et al.  Alien intracellular calcium chelators attenuate neurotransmitter release at the squid giant synapse , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[91]  E. M. Adler,et al.  Strategic location of calcium channels at transmitter release sites of frog neuromuscular synapses , 1990, Neuron.

[92]  R. Marc,et al.  Patterns of glutamate immunoreactivity in the goldfish retina , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[93]  A J Hudspeth,et al.  Colocalization of ion channels involved in frequency selectivity and synaptic transmission at presynaptic active zones of hair cells , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[94]  P. Greengard,et al.  Synapsins in the vertebrate retina: Absence from ribbon synapses and heterogeneous distribution among conventional synapses , 1990, Neuron.

[95]  M. Nowycky,et al.  Direct measurement of exocytosis and calcium currents in single vertebrate nerve terminals , 1990, Nature.

[96]  B. Vogt,et al.  Distribution of muscarinic acetylcholine receptors on processes of isolated retinal cells , 1989, The Journal of comparative neurology.

[97]  J W Moore,et al.  Identification of ionic currents at presynaptic nerve endings of the lizard. , 1989, The Journal of physiology.

[98]  K. Ikeda,et al.  The relationship between the number of synaptic vesicles and the amount of transmitter released , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[99]  J. Toyoda,et al.  Analysis of synaptic inputs to on-off amacrine cells of the carp retina , 1988, The Journal of general physiology.

[100]  J. Dowling The Retina: An Approachable Part of the Brain , 1988 .

[101]  J J Pysh,et al.  Time course and frequency dependence of synaptic vesicle depletion and recovery in electrically stimulated sympathetic ganglia , 1987, Journal of neurocytology.

[102]  W. Almers,et al.  Final steps in exocytosis observed in a cell with giant secretory granules. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[103]  R. Dacheux,et al.  The rod pathway in the rabbit retina: a depolarizing bipolar and amacrine cell , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[104]  R. Fesce,et al.  Measurement of quantal secretion induced by ouabain and its correlation with depletion of synaptic vesicles , 1985, The Journal of cell biology.

[105]  S. J. Smith,et al.  Calcium entry into voltage‐clamped presynaptic terminals of squid. , 1985, The Journal of physiology.

[106]  S. J. Smith,et al.  Calcium entry and transmitter release at voltage‐clamped nerve terminals of squid. , 1985, The Journal of physiology.

[107]  J. Walrond,et al.  Structure of axon terminals and active zones at synapses on lizard twitch and tonic muscle fibers , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[108]  M H Ellisman,et al.  Synaptic morphology and differences in sensitivity. , 1985, Science.

[109]  J. Heuser,et al.  Endocytosis of synaptic vesicle membrane at the frog neuromuscular junction , 1984, The Journal of cell biology.

[110]  N. Cooper,et al.  Tracer uptake by photoreceptor synaptic terminals. I. Dark-mediated effects. , 1983, Journal of ultrastructure research.

[111]  K. Ikeda,et al.  Possible temperature-dependent blockage of synaptic vesicle recycling induced by a single gene mutation in Drosophila. , 1983, Journal of neurobiology.

[112]  E Neher,et al.  Discrete changes of cell membrane capacitance observed under conditions of enhanced secretion in bovine adrenal chromaffin cells. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[113]  C. Zucker,et al.  Localization of synaptic and nonsynaptic nicotinic‐acetylcholine receptors in the goldfish retina , 1982, The Journal of comparative neurology.

[114]  J. Toyoda,et al.  Ionic mechanisms of two types of on-center bipolar cells in the carp retina. II. The responses to annular illumination , 1981, The Journal of general physiology.

[115]  R Llinás,et al.  Relationship between presynaptic calcium current and postsynaptic potential in squid giant synapse. , 1981, Biophysical journal.

[116]  T. Reese,et al.  Structural changes after transmitter release at the frog neuromuscular junction , 1981, The Journal of cell biology.

[117]  E. Kandel,et al.  Presynaptic membrane potential affects transmitter release in an identified neuron in Aplysia by modulating the Ca2+ and K+ currents. , 1980, Proceedings of the National Academy of Sciences of the United States of America.

[118]  J. Gillespie The effect of repetitive stimulation on the passive electrical properties of the presynaptic terminal of the squid giant synapse , 1979, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[119]  S. Hagiwara,et al.  The time course of cortical vesicle fusion in sea urchin eggs observed as membrane capacitance changes. , 1978, Developmental biology.

[120]  M. Charlton,et al.  Slow release of transmitter at the squid giant synapse , 1977, Neuroscience Letters.

[121]  JOHN W. Moore Membranes, ions, and impulses , 1976 .

[122]  S. Highstein,et al.  Depletion of vesicles and fatigue of transmission at a vertebrate central synapse , 1975, Brain Research.

[123]  A R Martin,et al.  Synaptic transfer at a vertebrate central nervous system synapse. , 1975, The Journal of physiology.

[124]  K Kusano,et al.  Depression and recovery of transmission at the squid giant synapse. , 1975, The Journal of physiology.

[125]  H. Atwood,et al.  Synaptic Vesicles: Selective Depletion in Crayfish Excitatory and Inhibitory Axons , 1972, Science.

[126]  H. Pease,et al.  On understanding the organisation of the retinal receptor synapses. , 1971, Brain research.

[127]  A. R. Freeman,et al.  Stimulation-Dependent Alterations in Peroxidase Uptake at Lobster Neuromuscular Junctions , 1971, Science.

[128]  F. Dodge,et al.  Co‐operative action of calcium ions in transmitter release at the neuromuscular junction , 1967, The Journal of physiology.

[129]  B. Katz,et al.  The release of acetylcholine from nerve endings by graded electric pulses , 1967, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[130]  A. Ames,et al.  REVERSIBLE AND IRREVERSIBLE CHANGES IN THE FINE STRUCTURE OF NERVOUS TISSUE DURING OXYGEN AND GLUCOSE DEPRIVATION , 1965, The Journal of cell biology.